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A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development

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Abstract

The intrinsic disorder is highly abundant in eukaryotic genomes. In the animal kingdom, numerous intrinsically disordered proteins (IDPs) have been characterized, especially in cell signalling and transcription regulation. An intrinsically disordered region often folds in different structures allowing an IDP to recognize and bind different partners at various binding interfaces. In contrast, there have only been a few reports of IDPs from the plant kingdom. Plant-specific GRAS proteins play critical and diverse roles in plant development and signalling and often act as integrators of signals from multiple plant growth regulatory inputs. Using computational and bioinformatics tools, we demonstrate here that the GRAS proteins are intrinsically disordered, thus forming the first functionally required unfoldome in the plant kingdom. Furthermore, the N-terminal domains of GRAS proteins are predicted to contain numerous Molecular Recognition Features (MoRFs), short interaction-prone segments that are located within extended disorder regions and are able to recognize their interacting partners and to undergo disorder-to-order transitions upon binding to these specific partners. Overlapping with the relatively conserved motifs in the N-terminal domains of GRAS proteins, these predicted MoRFs represent the potential protein–protein binding sites and may be involved in molecular recognition during plant development. This study enables us to propose a conceptual framework that guides future experimental approaches to understand structure–function relationships of the entire GRAS family.

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References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van der Straeten D, Peng JR, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94. doi:10.1126/science.1118642

    Article  PubMed  CAS  Google Scholar 

  • Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, Sablowski R, Ostergaard L (2010) Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev 24:2127–2132. doi:10.1101/gad.593410

    Article  PubMed  CAS  Google Scholar 

  • Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104:13839–13844. doi:10.1073/pnas.0706386104

    Article  PubMed  CAS  Google Scholar 

  • Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692. doi:10.1007/s00425-004-1203-z

    Article  PubMed  CAS  Google Scholar 

  • Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14:1269–1278

    PubMed  CAS  Google Scholar 

  • Cheng YG, Oldfield CJ, Meng JW, Romero P, Uversky VN, Dunker AK (2007) Mining alpha-helix-forming molecular recognition features with cross species sequence alignments. Biochemistry 46:13468–13477. doi:10.1021/bi7012273

    Article  PubMed  CAS  Google Scholar 

  • Cui HC, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425. doi:10.1126/science.1139531

    Article  PubMed  CAS  Google Scholar 

  • Czikkel BE, Maxwell DP (2007) NtGRAS1, a novel stress-induced member of the GRAS family in tobacco, localizes to the nucleus. J Plant Physiol 164:1220–1230. doi:10.1016/j.jplph.2006.07.010

    Article  PubMed  CAS  Google Scholar 

  • Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29:1916–1927. doi:10.1038/emboj.2010.75

    Article  PubMed  CAS  Google Scholar 

  • Day RB, Shibuya N, Minami E (2003) Identification and characterization of two new members of the GRAS gene family in rice responsive to N-acetylchitooligosaccharide elicitor. Biochim Biophys Acta-Gene Struct Exp 1625:261–268. doi:10.1016/s0167-4781(02)00626-7

    Article  CAS  Google Scholar 

  • Day RB, Tanabe S, Koshioka M, Mitsui T, Itoh H, Ueguchi-Tanaka M, Matsuoka M, Kaku H, Shibuya N, Minami E (2004) Two rice GRAS family genes responsive to N-acetylchitooligosaccharide elicitor are induced by phytoactive gibberellins: evidence for cross-talk between elicitor and gibberellin signaling in rice cells. Plant MolBiol 54:261–272

    CAS  Google Scholar 

  • de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484. doi:10.1038/nature06520

    Article  PubMed  Google Scholar 

  • Dunker AK, Uversky VN (2010) Drugs for ‘protein clouds’: targeting intrinsically disordered transcription factors. Curr Opin Pharmacol 10:782–788. doi:10.1016/j.coph.2010.09.005

    Article  PubMed  CAS  Google Scholar 

  • Dunker AK, Obradovic Z, Romero P, Garner EC, Brown CJ (2000) Intrinsic protein disorder in complete genomes. Genome Inform Ser Workshop Genome Inform 11:161–171

    PubMed  CAS  Google Scholar 

  • Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CR, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang CH, Kissinger CR, Bailey RW, Griswold MD, Chiu M, Garner EC, Obradovic Z (2001) Intrinsically disordered protein. J Mol Graphics Model 19:26–59

    Article  CAS  Google Scholar 

  • Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41:6573–6582. doi:10.1021/bi012159+

    Article  PubMed  CAS  Google Scholar 

  • Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) Flexible nets—the roles of intrinsic disorder in protein interaction networks. Febs J 272:5129–5148. doi:10.1111/j.1742-4658.2005.04948.x

    Article  PubMed  CAS  Google Scholar 

  • Dyson HJ, Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54–60

    Article  PubMed  CAS  Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681

    Article  PubMed  CAS  Google Scholar 

  • Feng SH, Martinez C, Gusmaroli G, Wang Y, Zhou JL, Wang F, Chen LY, Yu L, Iglesias-Pedraz JM, Kircher S, Schafer E, Fu XD, Fan LM, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479. doi:10.1038/nature06448

    Article  PubMed  CAS  Google Scholar 

  • Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222. doi:10.1093/nar/gkp985

    Article  PubMed  CAS  Google Scholar 

  • Fode B, Siemsen T, Thurow C, Weigel R, Gatz C (2008) The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters. Plant Cell 20:3122–3135. doi:10.1105/tpc.108.058974

    Article  PubMed  CAS  Google Scholar 

  • Fu XD, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng JR, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200. doi:10.1105/tpc.006197

    Article  PubMed  CAS  Google Scholar 

  • Fuxreiter M, Simon I, Friedrich P, Tompa P (2004) Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 338:1015–1026. doi:10.1016/j.jmb.2004.03.017

    Article  PubMed  CAS  Google Scholar 

  • Gallagher KL, Benfey PN (2009) Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J 57:785–797. doi:10.1111/j.1365-313X.2008.03735.x

    Article  PubMed  CAS  Google Scholar 

  • Gao MJ, Parkin IAP, Lydiate DJ, Hannoufa A (2004) An auxin-responsive SCARECROW-like transcriptional activator interacts with histone deacetylase. Plant Mol Biol 55:417–431

    Article  PubMed  CAS  Google Scholar 

  • Gleason C, Chaudhuri S, Yang TB, Munoz A, Poovaiah BW, Oldroyd GED (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149–1152. doi:10.1038/nature04812

    Article  PubMed  CAS  Google Scholar 

  • Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17:1175–1187. doi:10.1101/gad.260703

    Article  PubMed  CAS  Google Scholar 

  • Haynes C, Oldfield CJ, Ji F, Klitgord N, Cusick ME, Radivojac P, Uversky VN, Vidal M, Iakoucheva LM (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. Plos Comput Biol 2:890–901. doi:10.1371/journal.pcbi.0020100

    Article  CAS  Google Scholar 

  • Heo JO, Chang KS, Kim IA, Lee MH, Lee SA, Song SK, Lee MM, Lim J (2011) Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proc Natl Acad Sci USA 108:2166–2171. doi:10.1073/pnas.1012215108

    Article  PubMed  CAS  Google Scholar 

  • Hirano K, Asano K, Tsuji H, Kawamura M, Mori H, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2010) Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell 22:2680–2696. doi:10.1105/tpc.110.075549

    Article  PubMed  CAS  Google Scholar 

  • Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd GED (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signalling in medicago truncatula. Plant Cell 21:545–557. doi:10.1105/tpc.108.064501

    Article  PubMed  CAS  Google Scholar 

  • Hou XL, Lee LYC, Xia KF, Yen YY, Yu H (2010) DELLAs modulate jasmonate signalling via competitive binding to JAZs. Dev Cell 19:884–894. doi:10.1016/j.devcel.2010.10.024

    Article  PubMed  CAS  Google Scholar 

  • Hussain A, Cao DN, Cheng H, Wen ZL, Peng JR (2005) Identification of the conserved serine/threonine residues important for gibberellin-sensitivity of Arabidopsis RGL2 protein. Plant J 44:88–99. doi:10.1111/j.1365-313X.2005.02512.x

    Article  PubMed  CAS  Google Scholar 

  • Hussain A, Cao DN, Peng JR (2007) Identification of conserved tyrosine residues important for gibberellin sensitivity of Arabidopsis RGL2 protein. Planta 226:475–483. doi:10.1007/s00425-007-0497-z

    Article  PubMed  CAS  Google Scholar 

  • Iakoucheva LM, Radivojac P, Brown CJ, O’Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32:1037–1049. doi:10.1093/nar/gkh253

    Article  PubMed  CAS  Google Scholar 

  • Lam E, Benfey PN, Gilmartin PM, Fang RX, Chua NH (1989) Site-specific mutations alter invitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci USA 86:7890–7894

    Article  PubMed  CAS  Google Scholar 

  • Levy DE, Darnell JE (2002) STATs: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651–662. doi:10.1038/nrm909

    Article  PubMed  CAS  Google Scholar 

  • Li XY, Qian Q, Fu ZM, Wang YH, Xiong GS, Zeng DL, Wang XQ, Liu XF, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li JY (2003) Control of tillering in rice. Nature 422:618–621. doi:10.1038/nature01518

    Article  PubMed  CAS  Google Scholar 

  • Lim J, Jung JW, Lim CE, Lee MH, Kim BJ, Kim M, Bruce WB, Benfey PN (2005) Conservation and diversification of SCARECROW in maize. Plant Mol Biol 59:619–630. doi:10.1007/s11103-005-0578-y

    Article  PubMed  CAS  Google Scholar 

  • Liu JG, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK (2006) Intrinsic disorder in transcription factors. Biochemistry 45:6873–6888. doi:10.1021/bi0602718

    Article  PubMed  CAS  Google Scholar 

  • Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61:4011–4019. doi:10.1093/jxb/erq217

    Article  PubMed  CAS  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GED, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705. doi:10.1073/pnas.0400595101

    Article  PubMed  CAS  Google Scholar 

  • Mittag T, Kay LE, Forman-Kay JD (2010) Protein dynamics and conformational disorder in molecular recognition. J Mol Recognit 23:105–116. doi:10.1002/jmr.961

    PubMed  CAS  Google Scholar 

  • Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362:1043–1059. doi:10.1016/j.jmb.2006.07.087

    Article  PubMed  CAS  Google Scholar 

  • Mohan A, Sullivan WJ, Radivojac P, Dunker AK, Uversky VN (2008) Intrinsic disorder in pathogenic and non-pathogenic microbes: discovering and analyzing the unfoldomes of early-branching eukaryotes. Mol Biosyst 4:328–340. doi:10.1039/b719168e

    Article  PubMed  CAS  Google Scholar 

  • Morohashi K, Minami M, Takase H, Hotta Y, Hiratsuka K (2003) Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J Biol Chem 278:20865–20873. doi:10.1074/jbc.M301712200

    Article  PubMed  CAS  Google Scholar 

  • Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463. doi:10.1038/nature07519

    Article  PubMed  CAS  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  PubMed  CAS  Google Scholar 

  • Oldfield CJ, Cheng Y, Cortese MS, Brown CJ, Uversky VN, Dunker AK (2005) Comparing and combining predictors of mostly disordered proteins. Biochemistry 44:1989–2000. doi:10.1021/bi047993o

    Article  PubMed  CAS  Google Scholar 

  • Patil A, Nakamura H (2006) Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. Febs Lett 580:2041–2045. doi:10.1016/j.febslet.2006.03.003

    Article  PubMed  CAS  Google Scholar 

  • Peng K, Radivojac P, Vucetic S, Dunker AK, Obradovic Z (2006) Length-dependent prediction of protein intrinsic disorder. Bmc Bioinformatics 7. doi:10.1186/1471-2105/7/208

  • Promponas VJ, Enright AJ, Tsoka S, Kreil DP, Leroy C, Hamodrakas S, Sander C, Ouzounis CA (2000) CAST: an iterative algorithm for the complexity analysis of sequence tracts. Bioinformatics 16:915–922

    Article  PubMed  CAS  Google Scholar 

  • Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK (2007) Intrinsic disorder and functional proteomics. Biophys J 92:1439–1456. doi:10.1529/biophysj.106.094045

    Article  PubMed  CAS  Google Scholar 

  • Raikhel N (1992) Nuclear targeting in plants. Plant Physiol 100:1627–1632

    Article  PubMed  CAS  Google Scholar 

  • Rajani S, Sundaresan V (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 11:1914–1922

    Article  PubMed  CAS  Google Scholar 

  • Richards DE, Peng JR, Harberd NP (2000) Plant GRAS and metazoan STATs: one family? Bioessays 22:573–577

    Article  PubMed  CAS  Google Scholar 

  • Romero P, Obradovic Z, Li XH, Garner EC, Brown CJ, Dunker AK (2001) Sequence complexity of disordered protein. Proteins-Struct Funct Genet 42:38–48

    Article  PubMed  CAS  Google Scholar 

  • Sanchez C, Vielba JM, Ferro E, Covelo G, Sole A, Abarca D, De Mier BS, Diaz-Sala C (2007) Two SCARECROW-LIKE genes are induced in response to exogenous auxin in rooting-competent cuttings of distantly related forest species. Tree Physiol 27:1459–1470

    PubMed  CAS  Google Scholar 

  • Schlessinger A, Liu JF, Rost B (2007) Natively unstructured loops differ from other loops. Plos Comput Biol 3:1335–1346. doi:10.1371/journal.pcbi.0030140

    Article  CAS  Google Scholar 

  • Schumacher K, Schmitt T, Rossberg M, Schmitz C, Theres K (1999) The lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96:290–295

    Article  PubMed  CAS  Google Scholar 

  • Singh GP, Ganapathi M, Dash D (2007) Role of intrinsic disorder in transient interactions of hub proteins. Proteins-Struct Funct Bioinformatics 66:761–765. doi:10.1002/prot.21281

    Article  CAS  Google Scholar 

  • Stuurman J, Jaggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218. doi:10.1101/gad.230702

    Article  PubMed  CAS  Google Scholar 

  • Sun XL, Jones WT, Harvey D, Edwards PJB, Pascal SM, Kirk C, Considine T, Sheerin DJ, Rakonjac J, Oldfield CJ, Xue B, Dunker AK, Uversky VN (2010) N-terminal domains of DELLA proteins are intrinsically unstructured in the absence of interaction with GID1/gibberellic acid receptors. J Biol Chem 285:11557–11571. doi:10.1074/jbc.M109.027011

    Article  PubMed  CAS  Google Scholar 

  • Tian CG, Wan P, Sun SH, Li JY, Chen MS (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol 54:519–532

    Article  PubMed  CAS  Google Scholar 

  • Tong HN, Jin Y, Liu WB, Li F, Fang J, Yin YH, Qian Q, Zhu LH, Chu CC (2009) DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signalling in rice. Plant J 58:803–816. doi:10.1111/j.1365-313X.2009.03825.x

    Article  PubMed  CAS  Google Scholar 

  • Torres-Galea P, Huang LF, Chua NH, Bolle C (2006) The GRAS protein SCL13 is a positive regulator of phytochrome-dependent red light signaling, but can also modulate phytochrome A responses. Mol Genet Genomics 276:13–30. doi:10.1007/s00438-006-0123-y

    Article  PubMed  CAS  Google Scholar 

  • Triezenberg SJ (1995) Structure and function of transcriptional activation domains. Curr Opin Genet Dev 5:190–196

    Article  PubMed  CAS  Google Scholar 

  • Uversky VN (2010) The Mysterious unfoldome: structureless, underappreciated, yet vital part of any given proteome. J Biomed Biotechnol 2010:568068. doi:10.1155/2010/568068

  • Uversky VN (2011) Multitude of binding modes attainable by intrinsically disordered proteins: a portrait gallery of disorder-based complexes. Chem Soc Rev 40:1623–1634. doi:10.1039/c0cs00057d

    Article  PubMed  CAS  Google Scholar 

  • Uversky VN, Gillespie JR, Fink AL (2000) Why are “natively unfolded” proteins unstructured under physiologic conditions? Proteins-Struct Funct Genet 41:415–427

    Article  PubMed  CAS  Google Scholar 

  • Uversky VN, Oldfield CJ, Dunker AK (2005) Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signalling. J Mol Recognit 18:343–384. doi:10.1002/jmr.747

    Article  PubMed  CAS  Google Scholar 

  • Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK (2007a) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6:2351–2366. doi:10.1021/pr0701411

    Article  PubMed  CAS  Google Scholar 

  • Vacic V, Uversky VN, Dunker AK, Lonardi S (2007b) Composition profiler: a tool for discovery and visualization of amino acid composition differences. Bmc Bioinformatics 8. doi:10.1186/1471-2105-8-211

  • Vucetic S, Xie HB, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J Proteome Res 6:1899–1916. doi:10.1021/pr060393m

    Google Scholar 

  • Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293:321–331

    Article  PubMed  CAS  Google Scholar 

  • Wright PE, Dyson HJ (2009) Linking folding and binding. Curr Opin Struct Biol 19:31–38. doi:10.1016/j.sbi.2008.12.003

    Article  PubMed  CAS  Google Scholar 

  • Xie HB, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007a) Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6:1917–1932. doi:10.1021/pr060394e

    Google Scholar 

  • Xie HB, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN, Obradovic Z (2007b) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6:1882–1898. doi:10.1021/pr060392u

    Google Scholar 

  • Xue B, Oldfield CJ, Dunker AK, Uversky VN (2009) CDF it all: consensus prediction of intrinsically disordered proteins based on various cumulative distribution functions. Febs Lett 583:1469–1474. doi:10.1016/j.febslet.2009.03.070

    Article  PubMed  CAS  Google Scholar 

  • Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochimica et Biophysica Acta 1804. doi:10.1016/j.bbapap.2010.01.011

  • Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu JH, Heo JO, Lim J, Kamiya Y, Yamaguchi S, Sun TP (2011) SCARECROW-LIKE 3 promotes gibberellin signalling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci USA 108:2160–2165. doi:10.1073/pnas.1012232108

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We appreciate Dr. Predrag Radivojac for his help in predicting phosphorylation sites.

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Authors and Affiliations

  1. The New Zealand Institute for Plant and Food Research, Private Bag 11030, Palmerston North, New Zealand

    Xiaolin Sun & William T. Jones

  2. Department of Molecular Medicine, College of Medicine, University of South Florida, Tampa, FL, 33612, USA

    Bin Xue & Vladimir N. Uversky

  3. The New Zealand Institute for Plant and Food Research, Private Bag 92169, Auckland, New Zealand

    Erik Rikkerink

  4. Center for Computational Biology and Bioinformatics, Department of Biochemistry and Molecular Biology, School of Medicine, Indiana University, Indianapolis, IN, USA

    A. Keith Dunker

  5. Institute for Biological Instrumentation, Russian Academy of Sciences, 142290 Pushchino, Moscow Region, Russia

    Vladimir N. Uversky

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  1. Xiaolin Sun
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Correspondence to Xiaolin Sun or Vladimir N. Uversky.

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Sun, X., Xue, B., Jones, W.T. et al. A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol Biol 77, 205–223 (2011). https://doi.org/10.1007/s11103-011-9803-z

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